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The endogenous cannabinoid system controls extinction of aversive memories
Abstract
Acquisition and storage of aversive memories is one of the basic principles of central nervous systems throughout the animal kingdom. In the absence of reinforcement, the resulting behavioural response will gradually diminish to be finally extinct. Despite the importance of extinction, its cellular mechanisms are largely unknown. The cannabinoid receptor 1 (CB1) and endocannabinoids are present in memory-related brain areas and modulate memory. Here we show that the endogenous cannabinoid system has a central function in extinction of aversive memories. CB1-deficient mice showed strongly impaired short-term and long-term extinction in auditory fear-conditioning tests, with unaffected memory acquisition and consolidation. Treatment of wild-type mice with the CB1 antagonist SR141716A mimicked the phenotype of CB1-deficient mice, revealing that CB1 is required at the moment of memory extinction. Consistently, tone presentation during extinction trials resulted in elevated levels of endocannabinoids in the basolateral amygdala complex, a region known to control extinction of aversive memories. In the basolateral amygdala, endocannabinoids and CB1 were crucially involved in long-term depression of GABA (gamma-aminobutyric acid)-mediated inhibitory currents. We propose that endocannabinoids facilitate extinction of aversive memories through their selective inhibitory effects on local inhibitory networks in the amygdala.
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“Following their binding to central nervous system receptors (e.g.CB1 receptors), endocannabinoids have been shown, e.g., to reduce anxiety (Marsicano et al., 2002;Lutz et al., 2015) and increase food intake (Di Marzo et al., 2001).”
From Sleep restriction alters plasma endocannabinoids concentrations before but not after exercise in humans (2016) · cites this paper as Marsicano et al., 2002
In the citing paper
“Moreover, there is an emerging body of evidence demonstrating an important role for CB1 receptor-mediated endocannabinoid signaling in the extinction of aversive memories8.”
From Elevated brain cannabinoid CB1 receptor availability in post-traumatic stress disorder: A positron emission tomography study (2013) · cites this paper as [8]
In the citing paper
“As part of this protective role under aversive conditions, elevated EC signaling during stress has been shown to dampen the development of anxiety [12] and to regulate the encoding [13], retrieval [14] and extinction [15] of traumatic memories.”
From Plasma concentrations of endocannabinoids and related primary fatty acid amides in patients with post-traumatic stress disorder (2013) · cites this paper as [15]
In the citing paper
“Additionally, inhibition of FAAH facilitates long-term fear extinction and rescues deficient fear extinction in rodent models by enhancing AEA–CB1 (cannabinoid type 1) receptor signaling and synaptic plasticity in the BLA.”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [86]
In the citing paper
“Marsicano and colleagues reported elevated AEA and 2-AG BLA levels after extinction training in mice [86]”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [86]
In the citing paper
“One notable finding is that a CB1R-dependent form of synaptic plasticity in BLA [51,86], long-term depression of inhibitory GABAergic transmission (LTDi), is enhanced by FAAH KO [51] and by the FAAH inhibitor AM3506 at doses that promote extinction [50].”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [86]
In the citing paper
“and produced impairments in extinction learning (but not fear conditioning) by CB1R KO or systemic antagonist (SR141716A) administration [28,86]”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [86]
In the citing paper
“This suggests a scheme in which AEA released during extinction relieves a tonic inhibitory brake on BLA output neurons [50,51,86] necessary for the encoding of extinction memories [102] (Figure 2).”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [86]
In the citing paper
“The cannabinoid system is part of the complex circuitry that regulates anxiety and stress and is a crucial mediator of emotional learning (Marsicano et al, 2002;Viveros et al, 2005;Patel et al, 2005Patel et al, , 2005a; Laviolette and Grace, 2006;Varvel et al, 2007;Ganon-Elazar and Akirav, 2009;Lutz, 2009;Hill et al, 2009;Abush and Akirav, 2010;Akirav, 2011).”
From Cannabinoids prevent the development of behavioral and endocrine alterations in a rat model of intense stress (2012) · cites this paper as Marsicano et al, 2002
Citations
Cites
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444
Structure of a cannabinoid receptor and functional expression of the cloned cDNA
Matsuda, L. A., Lolait, S. J., Brownstein, M. J., Young, A. C., & Bonner, T. I. (1990) · Nature · doi:10.1038/346561a0 · Cited by 5,011
Genetic enhancement of learning and memory in mice
Tang, Y., Shimizu, E., Dubé, G., Rampon, C., Kerchner, G. A., Zhuo, M., Liu, G., & Tsien, J. Z. (1999) · Nature · doi:10.1038/43432 · Cited by 1,878
SR141716A, a potent and selective antagonist of the brain cannabinoid receptor
Rinaldi, M. L., Barth, F., Héaulme, M., Shire, D. J., Calandra, B., Congy, C., Martinez, S., Maruani, J., Neliat, G., Caput, D., et al. (1994) · FEBS Letters · doi:10.1016/0014-5793(94)00773-x · Cited by 1,762
Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses
Wilson, R. I., & Nicoll, R. A. (2001) · Nature · doi:10.1038/35069076 · Cited by 1,607
The role of ventromedial prefrontal cortex in the recovery of extinguished fear
Quirk, G. J., Russo, G. K., Barron, J. L., & Lebron, K. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06225.2000 · Cited by 957 · cited 1×
“; however, there is increasing evidence that some cellular pathways are specifically involved in extinction, but not in acquisition or consolidation of fear memorie”
BackgroundMarsicano, G., & Lutz, B. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00847.x · Cited by 937
Self-citationExtinction of emotional learning: contribution of medial prefrontal cortex
Morgan, M. A., Romanski, L. M., & LeDoux, J. E. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90241-c · Cited by 897 · cited 1×
“To confirm this assumption, we measured in C57BL/6J mice levels of the two major endocannabinoids, anandamide (AEA) and 2-arachidonoylglycerol (2-AG), in brain punches of the medial prefrontal cortex (mPFC) and the basolateral amygdala complex (BLAC), both of which are thought to have central roles in extinction of av…”
BackgroundOhno‐Shosaku, T., Maejima, T., & Kano, M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00247-1 · Cited by 874
Cannabinoid receptors and pain
Pertwee, R. G. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00031-9 · Cited by 741
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- Franklin, K. B. J. & Paxinos, G. The Mouse Brain (Academic, San Diego, 1997)
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Ständer, S., Schmelz, M., Metze, D., Luger, T. A., & Rukwied, R. (2005) · Journal of Dermatological Science · doi:10.1016/j.jdermsci.2005.01.007 · Cited by 303
Patel, S., Roelke, C. T., Rademacher, D. J., & Hillard, C. J. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03916.x · Cited by 297
Campolongo, P., Roozendaal, B., Trezza, V., Hauer, D., Schelling, G., McGaugh, J. L., & Cuomo, V. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900835106 · Cited by 294
Serum Endocannabinoid Content is Altered in Females with Depressive Disorders: A Preliminary Report
Hill, M., Miller, G., Ho, W.-S., Gorzalka, B., & Hillard, C. (2008) · Pharmacopsychiatry · doi:10.1055/s-2007-993211 · Cited by 292
Epigenetic Modifications in Stress Response Genes Associated With Childhood Trauma
Jiang, S., Postovit, L., Cattaneo, A., Binder, E. B., & Aitchison, K. J. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00808 · Cited by 288
van der Stelt, M., & Marzo, V. D. (2003) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2003.08.101 · Cited by 292
Possible endocannabinoid control of colorectal cancer growth
Ligresti, A., Bisogno, T., Matias, I., PETROCELLIS, L. D., Cascio, M. G., Cosenza, V., D’Argenio, G., Scaglione, G., Bifulco, M., Sorrentini, I., et al. (2003) · Gastroenterology · doi:10.1016/s0016-5085(03)00881-3 · Cited by 288
Self-citationFraser, G. A. (2009) · CNS Neuroscience & Therapeutics · doi:10.1111/j.1755-5949.2008.00071.x · Cited by 283
Drugs as instruments: A new framework for non-addictive psychoactive drug use
Müller, C. P., & Schumann, G. (2011) · Behavioral and Brain Sciences · doi:10.1017/s0140525x11000057 · Cited by 286
Role in Anxiety Behavior of the Endocannabinoid System in the Prefrontal Cortex
Rubino, T., Realini, N., Castiglioni, C., Guidali, C., Viganò, D., Marras, E., Petrosino, S., Perletti, G., Maccarrone, M., Marzo, V. D., et al. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm161 · Cited by 295
Bimodal control of stimulated food intake by the endocannabinoid system
Bellocchio, L., Lafenêtre, P., Cannich, A., Cota, D., Puente, N., Grandes, P., Chaouloff, F., Piazza, P. V., & Marsicano, G. (2010) · Nature Neuroscience · doi:10.1038/nn.2494 · Cited by 282
Self-citationMcCutcheon, J. E., & Marinelli, M. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06648.x · Cited by 299
Moreira, F. A., Kaiser, N., Monory, K., & Lutz, B. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.07.005 · Cited by 288
Self-citationAkirav, I., & Maroun, M. (2007) · Neural Plasticity · doi:10.1155/2007/30873 · Cited by 293
Best Practice & Research Clinical Endocrinology & Metabolism
Grieb, M. (2009) · Cited by 276
Substance P and pain chronicity
Zieglgänsberger, W. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2922-y · Cited by 283
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Jiménez-Blasco, D., Busquets-García, A., Hébert-Chatelain, É., Serrat, R., Vicente‐Gutiérrez, C., Ioannidou, C., Gómez-Sotres, P., López-Fabuel, I., Resch-Beusher, M., Resel, E., et al. (2020) · Nature · doi:10.1038/s41586-020-2470-y · Cited by 272
Self-citationAdult‐born neurons are necessary for extended contextual discrimination
Tronel, S., Belnoue, L., Grosjean, N., Revest, J., Piazza, P., Koehl, M., & Abrous, D. N. (2010) · Hippocampus · doi:10.1002/hipo.20895 · Cited by 274
Moreira, F. A., Grieb, M., & Lutz, B. (2009) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2008.09.003 · Cited by 277
Self-citationDifferential role of anandamide and 2-arachidonoylglycerol in memory and anxiety-like responses
Busquets-Garcia, A., Puighermanal, E., Pastor, A., de la Torre, R., Maldonado, R., & Ozaita, A. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.04.022 · Cited by 273
The cannabinoid system and pain
Woodhams, S. G., Chapman, V., Finn, D. P., Hohmann, A. G., & Neugebauer, V. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.06.015 · Cited by 285
The Endocannabinoid System Promotes Astroglial Differentiation by Acting on Neural Progenitor Cells
Aguado, T., Palazuelos, J., Monory, K., Stella, N., Cravatt, B. F., Lutz, B., Marsicano, G., Kokaia, Z., Guzmán, M., & Galve‐Roperh, I. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3101-05.2006 · Cited by 269
Self-citationSeeking a Spotless Mind: Extinction, Deconsolidation, and Erasure of Fear Memory
Maren, S. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.023 · Cited by 259
“Systemic administration of drugs that enhance cannabinoid signaling, such as the reuptake inhibitor AM404 and the CB1 receptor agonist WIN55212-2, have been reported to facilitate extinction learning under some conditions (Marsicano et al., 2002), although chronic administration of WIN55212-2 has recently been reporte…”
BackgroundDiana, M. A., & Marty, A. (2004) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0705726 · Cited by 266
Endocannabinoids Control the Induction of Cerebellar LTD
Safo, P. K., & Regehr, W. G. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.020 · Cited by 270
Circuitry for associative plasticity in the amygdala involves endocannabinoid signaling
Azad, S. C., Monory, K., Marsicano, G., Cravatt, B. F., Lutz, B., Zieglgänsberger, W., & Rammes, G. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.2134-04.2004 · Cited by 263
Self-citationde Bitencourt, R. M., Pamplona, F. A., & Takahashi, R. N. (2008) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2008.07.001 · Cited by 277
Amygdala Inhibitory Circuits Regulate Associative Fear Conditioning
Krabbe, S., Gründemann, J., & Lüthi, A. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.10.006 · Cited by 268
Hill, M. N., Patel, S., Campolongo, P., Tasker, J. G., Wotjak, C. T., & Bains, J. S. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4283-10.2010 · Cited by 255
Self-citationHill, M. N., Bierer, L. M., Makotkine, I., Golier, J. A., Galea, S., McEwen, B. S., Hillard, C. J., & Yehuda, R. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.08.004 · Cited by 256
Effects of Cannabinoids on Neurotransmission
Szabó, B., & Schlicker, E. (2005) · Springer eBooks · doi:10.1007/3-540-26573-2_11 · Cited by 256
Kullmann, D. M., Moreau, A. W., Bakiri, Y., & Nicholson, E. (2012) · Neuron · doi:10.1016/j.neuron.2012.07.030 · Cited by 234
Mechanisms of the anti-obesity effects of oxytocin in diet-induced obese rats
Deblon, N., Veyrat-Durebex, C., Bourgoin, L., Caillon, A., Bussier, A.-L., Petrosino, S., Piscitelli, F., Legros, J.-J., Geenen, V., Foti, M., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025565 · Cited by 254
Medicinal cannabis for psychiatric disorders: a clinically-focused systematic review
Sarris, J., Sinclair, J., Karamacoska, D., Davidson, M., & Firth, J. (2020) · BMC Psychiatry · doi:10.1186/s12888-019-2409-8 · Cited by 253
Melis, M., Perra, S., Muntoni, A. L., Pillolla, G., Lutz, B., Marsicano, G., Marzo, V. D., Gessa, G. L., & Pistis, M. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3502-04.2004 · Cited by 258
Self-citationCannabinoid Modulation of Amygdala Reactivity to Social Signals of Threat in Humans
Phan, K. L., Angstadt, M., Golden, J., Onyewuenyi, I., Popovska, A., & de Wit, H. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.5603-07.2008 · Cited by 251
Endocannabinoid-mediated long-term plasticity requires cAMP/PKA signaling and RIM1α
Chevaleyre, V., Heifets, B. D., Kaeser, P. S., Südhof, T. C., & Castillo, P. E. (2007) · Neuron · doi:10.1016/j.neuron.2007.05.020 · Cited by 261
Lin, C.-H., Yeh, S.-H., Lu, H.-Y., & Gean, P.-W. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-23-08310.2003 · Cited by 251
Hariri, A. R., Gorka, A. X., Hyde, L. W., Kimak, M. A., Halder, I., Ducci, F., Ferrell, R. E., Goldman, D. A., & Manuck, S. B. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.10.047 · Cited by 264
Molecular Components and Functions of the Endocannabinoid System in Mouse Prefrontal Cortex
Lafourcade, M., Elezgarai, I., Mato, S., Bakiri, Y., Grandes, P., & Manzoni, O. J. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000709 · Cited by 249
Hefner, K. R., Whittle, N., Juhasz, J., Norcross, M. A., Karlsson, R., Saksida, L. M., Bussey, T. J., Singewald, N., & Holmes, A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4904-07.2008 · Cited by 256
Hill, M. N., Carrier, E. J., McLaughlin, R. J., Morrish, A. C., Meier, S. E., Hillard, C. J., & Gorzalka, B. B. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05567.x · Cited by 246
Zhang, P. J., Ishiguro, H., Ohtsuki, T., Hess, J., Carillo, F., Walther, D. M., Onaivi, E. S., Arinami, T., & Uhl, G. R. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001560 · Cited by 250
Corticotropin-releasing hormone drives anandamide hydrolysis in the amygdala to promote anxiety
Gray, J. M., Vecchiarelli, H. A., Morena, M., Lee, T. T. Y., Hermanson, D. J., Kim, A. B., McLaughlin, R. J., Hassan, K. I., Kühne, C., Wotjak, C. T., et al. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.2737-14.2015 · Cited by 246
Self-citationPresynaptic Modulation by Endocannabinoids
Lovinger, D. M. (2007) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-74805-2_14 · Cited by 247
Overexpression of type-1 adenylyl cyclase in mouse forebrain enhances recognition memory and LTP
Wang, H., Ferguson, G. D., Pineda, V. V., Cundiff, P. E., & Storm, D. R. (2004) · Nature Neuroscience · doi:10.1038/nn1248 · Cited by 244
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Chhatwal, J. P., Rattiner, L. M., Davis, M., & Ressler, K. J. (2006) · Nature Neuroscience · doi:10.1038/nn1718 · Cited by 243
The endocannabinoid system in brain reward processes
Solinas, M., Goldberg, S. R., & Piomelli, D. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.130 · Cited by 251
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Garcia, R. (2017) · Learning & Memory · doi:10.1101/lm.044115.116 · Cited by 239
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Monory, K., Blaudzun, H., Massa, F., Kaiser, N., Lemberger, T., Schütz, G., Wotjak, C. T., Lutz, B., & Marsicano, G. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050269 · Cited by 261
Self-citationHill, M. N., Campolongo, P., Yehuda, R., & Patel, S. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.162 · Cited by 250
The endocannabinoid system in anxiety, fear memory and habituation
Ruehle, S., Rey, A. A., Remmers, F., & Lutz, B. (2011) · Journal of Psychopharmacology · doi:10.1177/0269881111408958 · Cited by 236
Self-citationThe psychiatric side-effects of rimonabant
Moreira, F. A., & Crippa, J. A. S. (2009) · Brazilian Journal of Psychiatry · doi:10.1590/s1516-44462009000200012 · Cited by 245
Nelson, S. B., & Turrigiano, G. G. (2008) · Neuron · doi:10.1016/j.neuron.2008.10.020 · Cited by 233
Price, D. A., Martinez, A. A., Seillier, A., Koek, W., Acosta, Y. P. V., Fernández, E., Strong, R., Lutz, B., Marsicano, G., Roberts, J. L., et al. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06764.x · Cited by 231
Self-citationMaejima, T., Oka, S., Hashimotodani, Y., Ohno‐Shosaku, T., Aiba, A., Wu, D., Waku, K., Sugiura, T., & Kano, M. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0945-05.2005 · Cited by 237
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Chanda, P. K., Gao, Y., Mark, L., Btesh, J., Strassle, B. W., Lu, P., Piesla, M. J., Zhang, M.-Y., Bingham, B., Uveges, A. J., et al. (2010) · Molecular Pharmacology · doi:10.1124/mol.110.068304 · Cited by 236
Ronesi, J. A., Gerdeman, G. L., & Lovinger, D. M. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5214-03.2004 · Cited by 229
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Micale, V., Marzo, V. D., Šulcová, A., Wotjak, C. T., & Drago, F. (2012) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2012.12.002 · Cited by 224
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CASALE, A. D., Sorice, S., Padovano, A., Simmaco, M., Ferracuti, S., Lamis, D. A., Rapinesi, C., Sani, G., Girardi, P., Kotzalidis, G. D., et al. (2018) · Current Neuropharmacology · doi:10.2174/1570159x16666180813155017 · Cited by 243
Makkar, S. R., Zhang, S. Q., & Cranney, J. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.53 · Cited by 230
Hill, M. N., Kumar, S. A., Filipski, S. B., Iverson, M., Stuhr, K. L., Keith, J. M., Cravatt, B. F., Hillard, C. J., Chattarji, S., & McEwen, B. S. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.90 · Cited by 222
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Castillo, P. E., Chiu, C. Q., & Carroll, R. C. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.01.006 · Cited by 222
The endocannabinoid system: emotion, learning and addiction
Moreira, F. A., & Lutz, B. (2008) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00104.x · Cited by 233
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Xu, J., Zhu, Y., Contractor, A., & Heinemann, S. F. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5716-08.2009 · Cited by 228
Azad, S. C., Eder, M., Marsicano, G., Lutz, B., Zieglgänsberger, W., & Rammes, G. (2003) · Learning & Memory · doi:10.1101/lm.53303 · Cited by 220
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Riedel, G., & Davies, S. N. (2005) · Springer eBooks · doi:10.1007/3-540-26573-2_15 · Cited by 219
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Vries, T. J. D., & Schoffelmeer, A. N. M. (2005) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2005.06.002 · Cited by 219
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Urigüen, L., Pérez-Rial, S., Ledent, C., Palomo, T., & Manzanares, J. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.01.003 · Cited by 218
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Kamprath, K., Marsicano, G., Tang, J., Monory, K., Bisogno, T., Marzo, V. D., Lutz, B., & Wotjak, C. T. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0153-06.2006 · Cited by 217
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Cannabis and psychiatric disorders: it is not only addiction
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Iversen, L. L. (2007) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195328240.001.0001 · Cited by 230
Quarta, C., Bellocchio, L., Mancini, G., Mazza, R., Cervino, C., Braulke, L. J., Fekete, C., Latorre, R., Nanni, C., Bucci, M., et al. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2010.02.015 · Cited by 217
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Metadata
- Authors
- Marsicano, G., Wotjak, C. T., Azad, S. C., Bisogno, T., Rammes, G., Cascio, M. G., Hermann, H., Tang, J., Hofmann, C., Zieglgänsberger, W., Di Marzo, V., & Lutz, B.
- Affiliations
- Max Planck Institute of Psychiatry (DE)
- LMU Klinikum (DE)
- Istituto di Chimica Biomolecolare (IT)
- Helmholtz Munich (DE)
- Corresponding author
- Lutz, Beat
- Venue
- Nature
- Published
- 2002-08
- Volume
- 418
- Issue
- 6897
- Pages
- 530-534
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1982291289
- Cited by
- 1,728
- References
- 30
- Citations by year
- 2026: 22 · 2025: 39 · 2024: 41 · 2023: 48 · 2022: 60 · 2021: 61 · 2020: 60 · 2019: 70 · 2018: 64 · 2017: 77 · 2016: 75 · 2015: 87 · 2014: 90 · 2013: 87 · 2012: 85
- FWCI
- 42.91
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- Topics
- Health Sciences › Medicine › Pharmacology (medical) › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- endocannabinoid system, CB1 receptor, CB1 knockout mice, fear extinction, auditory fear conditioning, basolateral amygdala, long-term depression, GABAergic inhibition, SR141716A, memory consolidation, inhibitory neural networks
- MeSH terms
- Rimonabant, Acoustic Stimulation, Amygdala, Animals, Cannabinoids, Conditioning, Classical, Electrophysiology, Extinction, Psychological, Fear, gamma-Aminobutyric Acid, Male, Memory, Mice, Inbred C57BL, Neuronal Plasticity, Neurons, Piperidines, Pyrazoles, Receptors, Drug, Synapses, Gene Deletion, Mice, Knockout, Receptors, Cannabinoid, Mice, Cannabinoid Receptor Modulators, In Vitro Techniques
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